Enhanced angiogenesis of gene-activated dermal equivalent for treatment of full thickness incisional wounds in a porcine model

Biomaterials

Volumn 31, Issue 28, 2010, Pages 7308-7320

  Guo, Rui ^a   Xu, Shaojun ^b   Ma, Lie ^a   Huang, Aibin ^a   Gao, Changyou ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Angiogenesis; Collagen chitosan scaffold; DNA complexes; Gene activated dermal equivalent; Incisional wounds; Vascular endothelial growth factor (VEGF)

Indexed keywords

ANGIOGENESIS; CHITOSAN SCAFFOLD; DERMAL EQUIVALENT; DNA COMPLEX; VASCULAR ENDOTHELIAL GROWTH FACTOR;

BIOACTIVITY; CHITIN; CHITOSAN; CHLORINE COMPOUNDS; COLLAGEN; DEFECTS; DNA; GENE ENCODING; GENE TRANSFER; PEPTIDES; POLYMERASE CHAIN REACTION; SCAFFOLDS; SELF ASSEMBLY; TENSILE STRENGTH;

DYES;

CHITOSAN; CHLORIDE; COLLAGEN; MESSENGER RNA; N,N,N TRIMETHYL CHITOSAN CHLORIDE; PLASMID DNA; SILICON; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN 165; BIOMATERIAL; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXPERIMENTAL PIG; FULL THICKNESS SKIN GRAFT; GENE ACTIVATION; GENE TARGETING; GENE VECTOR; GENETIC CODE; HISTOPATHOLOGY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SKIN BIOPSY; SKIN INJURY; SKIN TRANSPLANTATION; WESTERN BLOTTING; WOUND HEALING; ANIMAL; ARTIFICIAL SKIN; CHEMISTRY; CYTOLOGY; DERMIS; EVALUATION STUDY; GENETICS; HUMAN; MATERIALS TESTING; METABOLISM; PHYSIOLOGY; PROCEDURES; SWINE; TENSILE STRENGTH;

ANIMALS; BIOCOMPATIBLE MATERIALS; DERMIS; HUMANS; MATERIALS TESTING; NEOVASCULARIZATION, PHYSIOLOGIC; SKIN TRANSPLANTATION; SKIN, ARTIFICIAL; SWINE; TENSILE STRENGTH; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

SUIDAE; SUS;

EID: 77955266376     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2010.06.013     Document Type: Article

References (68)

1. Balasubramani M., Kumar T.R., Babu M. Skin substitutes: a review. Burns 2001, 27(5):534-544.
2. Singer A.J., Clark R.A. Cutaneous wound healing. N Engl J Med 1999, 341(10):738-746.
3. Hrabchak C., Flynn L., Woodhouse K.A. Biological skin substitutes for wound cover and closure. Expert Rev Med Devices 2006, 3(3):373-385.
4. Burke J.F., Yannas I.V., Quinby W.C., Bondoc C.C., Jung W.K. Successful use of a physiologically acceptable artificial skin in the treatment of extensive burn injury. Ann Surg 1981, 194(4):413-428.
5. Dagalakis N., Flink J., Stasikelis P., Burke J.F., Yannas I.V. Design of an artificial skin. Part III. Control of pore structure. J Biomed Mater Res 1980, 14(4):511-528.
6. Yannas I.V., Burke J.F. Design of an artificial skin. I. Basic design principles. J Biomed Mater Res 1980, 14(1):65-81.
7. Yannas I.V., Burke J.F., Gordon P.L., Huang C., Rubenstein R.H. Design of an artificial skin. II. Control of chemical composition. J Biomed Mater Res 1980, 14(2):107-132.
8. Yannas I.V., Burke J.F., Orgill D.P., Skrabut E.M. Wound tissue can utilize a polymeric template to synthesize a functional extension of skin. Science 1982, 215(4529):174-176.
9. Yannas I.V., Burke J.F., Warpehoski M., Stasikelis P., Skrabut E.M., Orgill D., et al. Prompt, long-term functional replacement of skin. Trans Am Soc Artif Intern Organs 1981, 27:19-23.
10. Shi Y.C., Ma L., Zhou J., Mao Z.W., Gao C.Y. Collagen/chitosan-silicone membrane bilayer scaffold as a dermal equivalent. Polym Adv Technol 2005, 16(11-12):789-794.
11. Ma L., Gao C., Mao Z., Zhou J., Shen J. Enhanced biological stability of collagen porous scaffolds by using amino acids as novel cross-linking bridges. Biomaterials 2004, 25(15):2997-3004.
12. Ma L., Gao C., Mao Z., Zhou J., Shen J., Hu X., et al. Collagen/chitosan porous scaffolds with improved biostability for skin tissue engineering. Biomaterials 2003, 24(26):4833-4841.
13. Gao C.Y., Wang D.Y., Shen J.C. Fabrication of porous collagen/chitosan scaffolds with controlling microstructure for dermal equivalent. Polym Adv Technol 2003, 14(6):373-379.
14. Ma L., Shi Y., Chen Y., Zhao H., Gao C., Han C. In vitro and in vivo biological performance of collagen-chitosan/silicone membrane bilayer dermal equivalent. J Mater Sci Mater Med 2007, 18(11):2185-2191.
15. Nillesen S.T., Geutjes P.J., Wismans R., Schalkwijk J., Daamen W.F., van Kuppevelt T.H. Increased angiogenesis and blood vessel maturation in acellular collagen-heparin scaffolds containing both FGF2 and VEGF. Biomaterials 2007, 28(6):1123-1131.
16. Richardson T.P., Peters M.C., Ennett A.B., Mooney D.J. Polymeric system for dual growth factor delivery. Nat Biotechnol 2001, 19(11):1029-1034.
17. Ehrbar M., Zeisberger S.M., Raeber G.P., Hubbell J.A., Schnell C., Zisch A.H. The role of actively released fibrin-conjugated VEGF for VEGF receptor 2 gene activation and the enhancement of angiogenesis. Biomaterials 2008, 29(11):1720-1729.
18. Shen Y.H., Shoichet M.S., Radisic M. Vascular endothelial growth factor immobilized in collagen scaffold promotes penetration and proliferation of endothelial cells. Acta Biomater 2008, 4(3):477-489.
19. Cao R., Brakenhielm E., Pawliuk R., Wariaro D., Post M.J., Wahlberg E., et al. Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2. Nat Med 2003, 9(5):604-613.
20. Perets A., Baruch Y., Weisbuch F., Shoshany G., Neufeld G., Cohen S. Enhancing the vascularization of three-dimensional porous alginate scaffolds by incorporating controlled release basic fibroblast growth factor microspheres. J Biomed Mater Res A 2003, 65(4):489-497.
21. Murphy W.L., Peters M.C., Kohn D.H., Mooney D.J. Sustained release of vascular endothelial growth factor from mineralized poly(lactide-co-glycolide) scaffolds for tissue engineering. Biomaterials 2000, 21(24):2521-2527.
22. Shea L.D., Smiley E., Bonadio J., Mooney D.J. DNA delivery from polymer matrices for tissue engineering. Nat Biotechnol 1999, 17(6):551-554.
23. Endo M., Kuroda S., Kondo H., Maruoka Y., Ohya K., Kasugai S. Bone regeneration by modified gene-activated matrix: effectiveness in segmental tibial defects in rats. Tissue Eng 2006, 12(3):489-497.
24. Chandler L.A., Gu D.L., Ma C., Gonzalez A.M., Doukas J., Nguyen T., et al. Matrix-enabled gene transfer for cutaneous wound repair. Wound Repair Regen 2000, 8(6):473-479.
25. Guo T., Zhao J., Chang J., Ding Z., Hong H., Chen J., et al. Porous chitosan-gelatin scaffold containing plasmid DNA encoding transforming growth factor-beta1 for chondrocytes proliferation. Biomaterials 2006, 27(7):1095-1103.
26. Tyrone J.W., Mogford J.E., Chandler L.A., Ma C., Xia Y., Pierce G.F., et al. Collagen-embedded platelet-derived growth factor DNA plasmid promotes wound healing in a dermal ulcer model. J Surg Res 2000, 93(2):230-236.
27. Hijjawi J., Mogford J.E., Chandler L.A., Cross K.J., Said H., Sosnowski B.A., et al. Platelet-derived growth factor B, but not fibroblast growth factor 2, plasmid DNA improves survival of ischemic myocutaneous flaps. Arch Surg 2004, 139(2):142-147.
28. Chandler L.A., Sosnowski B.A. Gene therapy for cutaneous wound repair. Wounds 2004, 16(1):1-9.
29. Ahrendt G., Chickering D.E., Ranieri J.P. Angiogenic growth factors: a review for tissue engineering. Tissue Eng 1998, 4(2):117-130.
30. Boontheekul T., Mooney D.J. Protein-based signaling systems in tissue engineering. Curr Opin Biotechnol 2003, 14(5):559-565.
31. Mao Z.W., Ma L., Jiang Y., Yan M., Gao C.Y., Shen J.C. N,N,N-Trimethylchitosan chloride as a gene vector: synthesis and application. Macromol Biosci 2007, 7(6):855-863.
32. Mao Z., Shi H., Guo R., Ma L., Gao C., Han C., et al. Enhanced angiogenesis of porous collagen scaffolds by incorporation of TMC/DNA complexes encoding vascular endothelial growth factor. Acta Biomater 2009, 5(8):2983-2994.
33. Mao H.-Q., Roy K., Troung-Le V.L., Janes K.A., Lin K.Y., Wang Y., et al. Chitosan-DNA nanoparticles as gene carriers: synthesis, characterization and transfection efficiency. J Control Release 2001, 70(3):399-421.
34. Springer M.L., Chen A.S., Kraft P.E., Bednarski M., Blau H.M. VEGF gene delivery to muscle: potential role for vasculogenesis in adults. Mol Cell 1998, 2(5):549-558.
35. Reno C., Marchuk L., Sciore P., Frank C.B., Hart D.A. Rapid isolation of total RNA from small samples of hypocellular, dense connective tissues. Biotechniques 1997, 22(6):1082-1086.
36. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45.
37. Peter X.M., Zhang R.Y. Synthetic nano-scale fibrous extracellular matrix. J Biomed Mater Res 1999, 46(1):60-72.
38. Benjamin L.E., Hemo I., Keshet E. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 1988, 125:1591-1598.
39. Trentin D., Hall H., Wechsler S., Hubbell J.A. Peptide-matrix-mediated gene transfer of an oxygen-insensitive hypoxia-inducible factor-1alpha variant for local induction of angiogenesis. Proc Natl Acad Sci U S A 2006, 103(8):2506-2511.
40. Kanzler M.H., Gorsulowsky D.C., Swanson N.A. Basic mechanisms in the healing cutaneous wound. J Dermatol Surg Oncol 1986, 12(11):1156-1164.
41. Druecke D., Lamme E.N., Hermann S., Pieper J., May P.S., Steinau H.U., et al. Modulation of scar tissue formation using different dermal regeneration templates in the treatment of experimental full-thickness wounds. Wound Repair Regen 2004, 12(5):518-527.
42. Lam P.K., Chan E.S., Liew C.T., Lau C., Yen S.C., King W.W. Combination of a new composite biocampatible skin graft on the neodermis of artificial skin in an animal model. ANZ J Surg 2002, 72(5):360-363.
43. Morimoto N., Suzuki S., Kim B.M., Morota K., Takahashi Y., Nishimura Y. In vivo cultured skin composed of two-layer collagen sponges with preconfluent cells. Ann Plast Surg 2001, 47(1):74-81. discussion 81-82.
44. Ophof R., Maltha J.C., Von den Hoff J.W., Kuijpers-Jagtman A.M. Histologic evaluation of skin-derived and collagen-based substrates implanted in palatal wounds. Wound Repair Regen 2004, 12(5):528-538.
45. Wood F.M., Stoner M.L., Fowler B.V., Fear M.W. The use of a non-cultured autologous cell suspension and integra dermal regeneration template to repair full-thickness skin wounds in a porcine model: a one-step process. Burns 2007, 33(6):693-700.
46. Siedler S., Schuller-Petrovic S. Allogenic keratinocytes suspended in human fibrin glue used for wound healing support in chronic leg ulcers. Arch Dermatol 2000, 136(5):676-678.
47. King S.R., Hickerson W.L., Proctor K.G. Beneficial actions of exogenous hyaluronic acid on wound healing. Surgery 1991, 109(1):76-84.
48. Murashita T., Nakayama Y., Hirano T., Ohashi S. Acceleration of granulation tissue ingrowth by hyaluronic acid in artificial skin. Br J Plast Surg 1996, 49(1):58-63.
49. Gomathi K., Gopinath D., Rafiuddin Ahmed M., Jayakumar R. Quercetin incorporated collagen matrices for dermal wound healing processes in rat. Biomaterials 2003, 24(16):2767-2772.
50. Ruszczak Z., Schwartz R.A. Modern aspects of wound healing: an update. Dermatol Surg 2000, 26(3):219-229.
51. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med 2000, 6(4):389-395.
52. Tsurumi Y., Takeshita S., Chen D., Kearney M., Rossow S.T., Passeri J., et al. Direct intramuscular gene transfer of naked DNA encoding vascular endothelial growth factor augments collateral development and tissue perfusion. Circulation 1996, 94(12):3281-3290.
53. Huang Y.C., Kaigler D., Rice K.G., Krebsbach P.H., Mooney D.J. Combined angiogenic and osteogenic factor delivery enhances bone marrow stromal cell-driven bone regeneration. J Bone Miner Res 2005, 20(5):848-857.
54. Ramsay E., Hadgraft J., Birchall J., Gumbleton M. Examination of the biophysical interaction between plasmid DNA and the polycations, polylysine and polyornithine, as a basis for their differential gene transfection in-vitro. Int J Pharm 2000, 210(1-2):97-107.
55. Zaitsev S., Cartier R., Vyborov O., Sukhorukov G., Paulke B.R., Haberland A., et al. Polyelectrolyte nanoparticles mediate vascular gene delivery. Pharm Res 2004, 21(9):1656-1661.
56. Sullivan T.P., Eaglstein W.H., Davis S.C., Mertz P. The pig as a model for human wound healing. Wound Repair Regen 2001, 9(2):66-76.
57. O'Brien F.J., Harley B.A., Yannas I.V., Gibson L.J. The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials 2005, 26(4):433-441.
58. Valarmathi M.T., Davis J.M., Yost M.J., Goodwin R.L., Potts J.D. A three-dimensional model of vasculogenesis. Biomaterials 2009, 30(6):1098-1112.
59. Davies N., Dobner S., Bezuidenhout D., Schmidt C., Beck M., Zisch A.H., et al. The dosage dependence of VEGF stimulation on scaffold neovascularisation. Biomaterials 2008, 29(26):3531-3538.
60. Ozawa C.R., Banfi A., Glazer N.L., Thurston G., Springer M.L., Kraft P.E., et al. Microenvironmental VEGF concentration, not total dose, determines a threshold between normal and aberrant angiogenesis. J Clin Invest 2004, 113(4):516-527.
61. Barboni B., Turriani M., Galeati G., Spinaci M., Bacci M.L., Forni M., et al. Vascular endothelial growth factor production in growing pig antral follicles. Biol Reprod 2000, 63(3):858-864.
62. von Degenfeld G., Banfi A., Springer M.L., Wagner R.A., Jacobi J., Ozawa C.R., et al. Microenvironmental VEGF distribution is critical for stable and functional vessel growth in ischemia. FASEB J 2006, 20(14):2657-2659.
63. Benjamin L.E., Keshet E. Conditional switching of vascular endothelial growth factor (VEGF) expression in tumors: induction of endothelial cell shedding and regression of hemangioblastoma-like vessels by VEGF withdrawal. Proc Natl Acad Sci U S A 1997, 94(16):8761-8766.
64. Dor Y., Djonov V., Abramovitch R., Itin A., Fishman G.I., Carmeliet P., et al. Conditional switching of VEGF provides new insights into adult neovascularization and pro-angiogenic therapy. EMBO J 2002, 21(8):1939-1947.
65. Wilcke I., Lohmeyer J.A., Liu S., Condurache A., Kruger S., Mailander P., et al. VEGF(165) and bFGF protein-based therapy in a slow release system to improve angiogenesis in a bioartificial dermal substitute in vitro and in vivo. Langenbecks Arch Surg 2007, 392(3):305-314.
66. Miquerol L., Langille B.L., Nagy A. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 2000, 127(18):3941-3946.
67. Carney D.H., Mann R., Redin W.R., Pernia S.D., Berry D., Heggers J.P., et al. Enhancement of incisional wound healing and neovascularization in normal rats by thrombin and synthetic thrombin receptor-activating peptides. J Clin Invest 1992, 89(5):1469-1477.
68. Scardino M.S., Swaim S.F., Morse B.S., Sartin E.A., Wright J.C., Hoffman C.E. Evaluation of fibrin sealants in cutaneous wound closure. J Biomed Mater Res 1999, 48(3):315-321.